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1 Annals of the Royal College of Surgeons of England (1984) vol. 66 Pretibial myxoedema G STEWART FRCS Lecturer in Surgery THE LATE J B KINMONTH MS, FRCS N L BROWSE MD, FRCS Professor of Surgery St Thomas' Hospital, London Key words: HYPERTHYROIDISM; PRETIBIAL MMYXOEDEMA; LYMPHATIC SYSTE,M; HYROID ACROPACHY Summary This paper reviews the clinical, endocrine and lymphatic status of 6 patients with pretibial myxoedema. The lymphatics were studied to determine whether they were involved in the pathogenesis of the disease. The main lymph trunks were normal although there was occasionally some collateralflow and some of the lymph nodes had small irregular filling defects. These changes suggest compression of the lymphatics by the myxomatous material and the deposition of mucinous material in the lymph nodes. There was no evidence of a primary lymphatic abnormality. Introduction Pretibial myxoedema (PTM) (syn. myxoedema circumscriptum thyrotoxicum) is said to occur in 1-40/ of patients with hyperthyroidism but may also develop after its correction (1, 2). Cairns (3) states that it is not found in patients with spontaneous hypothyroidism but that it may develop in patients who have been made hypothyroid by treatment. It is one of a triad of lesions associated with auto-immune thyroid disease (4), pretibial myxoedema, exophthalmosthe commonest of the three, and thyroid acropachy the rarest. In the past 11 years we have studied the lymphatics of the limbs of 6 patients with PTM. This paper describes their clinical, endocrine and lymphatic status, each section preceded by a general review based upon the published literature. Clinical features Pretibial myxoedema develops in the subcutaneous tissues and skin of the anterolateral aspect of the lower limbs, and occasionally of the feet and the back of the legs (3). The upper limbs are rarely affected (5). It first appears as cutaneous nodules, which usually have a pink tinge, but sometimes a yellow or waxy appearance. Localised hypertrichosis is often seen and the hair follicles may become indented causing a 'peau d'orange' appearance. Cairns (3) described three clinical appearances: (1) Sharply circumscribed, localised, nodular or tuberous like lesions. (2) A diffuse thickening similar to a hard non-pitting oedema. (3) An elephantitic leg caused by multiple skin nodules and extensive subcutaneous infiltration. The lesions vary in appearances from patient to patient and may also vary in the same patient with time. The early Correspondence to: G Stewart FRCS, Department of Surgery, St Thomas' Hospital, London SEI 7EH. The Editor would welcome any comments on this paper by readers small nodules, occasionally mistaken for erythema nodosum, may develop into extensive areas of irregular swelling. Our 6 patients showed all three types of lesion. Two presented with localised nodules which progressed to diffuse thickening over 1 and 2 years respectively. Three presented with diffuse thickening, one mild, and two moderately severe with changes involving the whole of the anterior aspect of the lower leg. The sixth patient presented with nodular lesions, first thought to be erythema nodosum, which rapidly became confluent, The infiltration progressed rapidly to an elephantiasis-like lesion within 2 years. These changes are illustrated in Fig. 1. Fig la shows the nodular and diffuse thickening shortly after she presented in Fig. lb and lc show the remarkable change that had occurred by 1981; elephantiasis-like legs with protruding nodules and crevices on the anterior aspect of the lower leg spreading around the ankles, and over the feet and toes. Exophthalmos Four of our patients had exophthalmos, one mildly, two moderately severely and one, a particularly severe form, required bilateral orbital decompression. Both the patients with moderately severe exophthalmos were treated successfully with oral steroids. The incidence of exophthalmos in patients with thyrotoxicosis is difficult to assess (6) although it is said to be between 40 and 50O" (6,7). This, however, includes all eye changes from minimal lid lag to severe orbital changes. The presence of established exophthalmos in 4 of our 6 patients is probably higher than the expected incidence of this condition. Thyroid acropachy is a rare condition occurring in less than 10 of patients with hyperthyroidism. It is characterised by digital clubbing and thickening of the long bones of the fingers and arms (8). The X-ray appearances are diagnostic (9) and consist of periosteal new bone formation having an irregular, lacey, and at times bubbly appearance, in the middiaphyseal areas of the metatarsals, metacarpals and phalanges. These changes are often first detected in the first metacarpals. The trabeculae of the new bone lies at right angles to the axis of the bone so differing from that of pulmonary osteo-arthropathy in which the new layer of subperiosteal bone is longitudinally apposed to the shaft of the long hand bones. One of our patients had.the textbook clinical and radiological features of thyroid acropachy. Fig 2a shows obvious thickening of the proximal phalanx of the second and the middle phalanx of the fourth fingers, and Fig. 2b the x-ray changes. This was the patient illustrated in Fig. 1 who developed the most severe form of pretibial myxoedema. The hands of the other 5 patients were normal.
2 392 G Stewart Endocrine features It is thought that pretibial myxoedema follows a period of hyperthyroidism and is related to the presence of a long acting thyroid stimulator (LATS). Four of our patients were initially thyrotoxic but all became hypothyroid after treatment and required replacement therapy. The fifth patient was hypothyroid from the start of her management and has never had any clinical or laboratory evidence of hyperthyroidism. The sixth patient was first seen in the hyperthyroid phase of Hashimoto's thyroiditis. She was treated with radioactive iodine but her thyroid activity was difficult to control and she had several further episodes of hyperthyroidism, though she presently requires thyroxine replacement therapy. Lynch (10) has reviewed several series of patients with PTM and measured the serum LATS in 4 of his own patients. The serum of all of his own cases contained LATS. He suggested that the aetiology was more closely related to the presence of LATS and associated antibodies than the hyperthyroidism itself, and that PTM may occur in nonthyrotoxic thyroid disease. Four of our cases had circulating thyroid antibodies but the patient presenting with primary hypothyroidism had none. Antibodies were not measured in the sixth patient. The interval between the onset of symptoms and signs of thyroid disease and pretibial myxoedema varied (Table). One patient developed both conditions at the start of her illness. Three developed the pretibial myxoedema between 2 and 4 years later and one 8 years later. The sixth patient developed pretibial myxoedema 6 years before the diagnosis of primary hypothyroidism was made. In all but the second patient the thyroid status was normal when the leg swelling began to appear. In this patient there was no evidence of regression associated with control of the hyperthyroidism. Lymphographic features The state of the lymphatics in legs with PTM has never been documented. The lymphographic findings in our 6 patients are summarised below. The lymphangiographs were so close to normal that we do not consider them worthy of illustration. The changes we describe are our subjective interpretation based upon our experience of over 2000 lymphographs. (1) The main lymph trunks were normal. (2) Where they traversed an area of myxoedema there was occasionally some flow of the Lipiodol into collateral channels. (3) Some of the inguinal and iliac lymph nodes had a ragged appearance and contained a number of small irregular filling defects. Some were slightly enlarged (Fig. 3). The changes we have described would be consistent with the hypothesis that the lymphatics in the affected areas of the leg are occasionally blocked or compressed by the myxomatous material and that mucinous deposits may occur in the lymph nodes. We have found no evidence of any primary lymphatic abnormality in PTM. Histological features Pretibial myxoedema is caused by a mucinous infiltration of the deeper parts of the dermis, followed by a reactive fibroblastic proliferation. The mucin separates the collagen fibres of the dermis and makes the skin very thick (11). Slides stained with haematoxylin and eosin show large pale areas in the deeper part of the dermis which stain deep blue when stained for mucin with Alcian Blue. Skin biopsies were taken from 3 of our patients. All showed the typical histopathological features of PTM (Fig. 4). Treatment Because of the variable behaviour of the PTM lesions which tend to pass slowly through periods of remission or excerbation, the effect of treatment is difficult to assess. The only form of medical treatment shown to have a consistent effect on pretibial myxoedema is the local application of steroid preparations aided by a plastic occlusion dressing (3). The rationale for this treatment is based on the evidence that cortisone depresses the synthesis of mucopolysaccharides. Paver (12) improved his results by injecting a b c 1 Two stages of a rapidly progressing, severe case of pretibial myxoedema (Patient 6). (a) 1978: diffuse thickening over the leg and foot. (b) 1981: progression of the disease to an elephantiasis-like appearance, gross swelling, thickening and multiple nodules. (c) 1981: a close-up view illustrating the nodularity and the depth of the crevices.
3 393 al 3 A lymphadenograph of a patient with pretibial myxoedema showing multiple small filling defects within slightly enlarged and ragged inguinal and iliac lymph nodes (Patient 6). i, ~ ~ 1A area 4 H and E stain of the skin and subcutaneous tissue from of pretibial myxoedema showing large an gaps in the dermis filled by the mucinous infiltration. steroids into the lesions and adding hyaluronidase and compression bandages. He suggested that steroids, hyaluronidase and pressure had different, but synergistic, mechanisms of action. The success of may also be related to the possibility that PTM is an auto-immune phenomenon. Other forms of immuno-suppression such as systemic steroids and azathioprine have been tried with varying results. For example, Dandona et al. successfully treated several patients with acute fulminating exophthalmos and acutely progressing PTM with plasmapheresis followed by systemic corticosteroids and azathioprine (13). However, 2 Thyroid acropachy. (a) The hands of Patient 6 showing thickening of the proximal phalanges, second and third fingers, and the middle phalanx of the fourth finger. There is also clubbing most noticeable in the second fingers of both hands and the middle finger ofthe right hand. (b) An x-ray ofthe hands shown in Fig. 2a. There is dense periosteal new bone formation along the shafts of a number of the proximal and middle phalanges, (corresponding to the visible swelling of the fingers). There are also minor changes in both first metacarpals. (c) A macroradiograph illustrating the periosteal new bone formation and the radial direction of its trabeculae.
4 394 G Stewart TABLE Patient 1. J B 2. AC 3. CB 4. EB Initial diagnosis andyear of onset HT Hypothyroidism, 6. H W Hashimoto's thyroiditis, 1977 Thyroid antibody status Not done Negative Treatment Subtoal thyroidectomy, radioactive iodine Thyroxine rear of control of hyperthyroidism or hypothyroidism Year of onset of pretibial myxoedema and treatment, 1971 (7), 1971, none, +oral steroids* 1967, none 1977, oral steroids* Stiate of legs at review Unchanged Almost resolved, minimal skin changes Moderately worse Unchanged No evidence of PTM Severe PTM, * Oral steroids given to treat eye problems. Lewis et al. (14) did not find this regimen helpful and Harvard (15) states that it only helps the acute and rapidly progressive exophthalmos. It is difficult to imagine how plasmapheresis can reverse established PTM. One of our patients was treated with systemic steroids. Her PTM which was in an early stage at that time, completely resolved. It recurred 6 months later and has now progressed to the extreme state shown in Fig lb and lc. Neither local nor systemic steroids have had any effect on the skin lesions during the past year. Three patients have been treated with. In 2 there was no effect but the third almost completely resolved after 4 months treatment with locally applied steroids under occlusive dressings. One patient with the moderately severe diffuse variety had no treatment and her PTM has progressed. Conversely the other patient with mild diffuse thickened variety who had no treatment had a complete spontaneous remission 5 years later. She was the patient who presented with myxoedema without a history of hyperthyroidism. Patients with severe PTM may seek surgical intervention but as recurrence after excision, with or without split skin grafting, has been reported (16), surgery should only be used in chronic severe cases after a proper trial of medical therapy. Patient No. 6 was offered two forms of surgery; a paring off of the cutaneous nodules and thickened skin, which can be a most successful way of treating the keloid nodules that develop in old skin grafts in lymphoedematous legs, and total excision of the skin and fat with replacement by split skin grafts (Charles' operation). After much thought the patient decided against any surgical therapy. Discussion The pathogenesis of PTM is unknown and many causative mechanisms have been proposed. The most commonly accepted hypothesis is that PTM is caused by a local autoimmune reaction. Several groups have reported an association between LATS and pretibial myxoedema (17-19). Hetzel (19) measured the plasma level of LATS in 5 patients with thyrotoxicosis and pretibial myxoedema. He found that a worsening of the pretibial myxoedema was associated with a rise, and remission with a fall, in the level of plasma LATS. He suggested there was a close, if not direct, causal relationship between LATS and pretibial myxoedema. McKenzie (4) has implicated other circulating thyroid stimulating IgG molecules such as LATS protector and human thyroid stimulator. He stated that all these changes might reflect a single spectrum of polyclonal IgG molecules collectively known as thyroid stimulating hormone receptor antibodies, all of which are involved in the pathogenesis of Graves' disease and pretibial myxoedema. It has been suggested that all patients with thyroid dysfunction associated with conditions such as exophthalmos and pretibial myxoedema have auto-immune thyroid disease. They may, at different times, display hyperthyroidism, hypothyroidism, or be euthyroid but can be differentiated from other patients with thyroid disease by the presence of auto-antibodies. They are likely to be HLA/Dr3 positive and are therefore immune responders with a potentiality for producing auto-antibodies (20). The constancy with which PTM is confined to the lower limbs suggests that a local tissue factor is involved. In 1968 Sisson showed that the skin lesions of PTM contained from 6 to 16 times the normal amount of hyaluronic acid (21). From and colleagues (22) suggested that this was caused by a local metabolic effect of LATS on the cells in the ground substance of the connective tissue. Cheung (23) postulated that the increased synthesis of mucopolysaccharide ground substance found in pretibial myxoedema came from the fibroblasts. When he cultured and incubated fibroblasts from the pretibial area of PTM patients and normal individuals in serum from PTM patients, they synthesised 2-3 times the amount of hyaluronic acid produced by fibroblasts from other areas. When fibroblasts from normal or PTM patients from any areas were incubated with normal serum the synthesis of hyaluronic acid was unchanged. Cheung's findings and hypothesis have been confirmed by Jollife (24) in 'in vitro' experiments and by Konrad (25) in morphological studies. These studies suggest that there is both a systemic serum borne effect and a local increased sensitivity, though what should make the skin of the anterior aspect of the lower limb different and susceptible is difficult to imagine. The name pretibial myxoedema has been used for many years and is unlikely to be changed. It is a bad name, for the word myxoedema is also used to describe the clinical features of hypothyroidism, and the word oedema is usually used in a clinical context to imply an excess of watery fluid in the interstitial spaces. There is no excess water in limbs with pretibial myxoedema, just an interstitial mucinous (myxomatous) infiltration. The condition might be better called pretibial 'mucinous infiltration'.
5 References I Trotter WR, Eden KC. Localised pretibial myxoedema in association with toxic goiter. QJ Med 1942;35: Caravati CM, Richardson DR, Wood BT et al. Cutaneous manifestations of hyperthyroidism. South Med J 1969;62: Cairns RJ Pretibial myxoedema In: Rook Wilkinson and Ebling, eds. Textbook of dermatology, 3rd ed. Oxford: Blackwell, 1979: McKenzie JM, Zakarisa M, Bonnyns M. Graves disease. Med Clin North Am 1975;59,5: Cohen BD, Benua RS, Rawson RW. Localised myxoedema involving the upper extremities. Arch Int Med 1963;1 1: Werner SC. The thyroid: a fundamental and clinical text, 4th ed. New York: Harper and Row, 1978: Croft DN, Williams JO, Coakley AJ. Dysthyroid eye disease. In: Perkins and Hill. Scientific foundations of ophthalmology. London: Heinemann, 1977: Goette DK. Thyroid acropachy. Arch Dermatol 1980; 116: Moule B, Grant MC, Boyle IT, May H. Thyroid acropachy. Clin Radiol 1970;2: Lynch PJ, MaizeJC, SissonJC. Pretibial myxoedema and nonthyrotoxic thyroid disease. Arch Dermatol ; 107 (1): Lever WF. Histopathology of the skin, 5th ed. Philadelphia, Toronto: JB Lippincott Co, 1975: Paver WKA. Treatment of pretibial myxoedema and cutaneous myxoid cysts. AustralasJ Dermatol 1977;18: Dandona P, Marshall NJ, Bidey SP, Nathan A, Havard CWH. Successful treatment of exophthalmos and pretibial myxoedema with plasmapheresis. Br Med J 1979; 1: Lewis RA, Slater N, Croft DN. Exophthalmos and pretibial myxoedema not responding to plasmapheresis. Br Med J 1979;2: Prelibial myxoedema Havard CWH. Progress in endocrine exophthalmos. Br Med J 1979; 1: Kucer KA, Luscombe HA, Young CK. Pretibial myxoedema. Arch Dermatol 1980; 116: Carneiro L, Dorrington KH, Munro DS. Relationship between long acting thyroid stimulator and thyroid function in thyrotoxicosis. Lancet 1966;2: Pinchera A, Pinchera MG, StanburyJB. Thyrotropin and long acting thyroid stimulator assays in thyroid disease. J Clin Endocrinol Metab 1965;25: Hetzel BS, Wall JR. Pretibial myxoedema. Australas J Dermatol 1969; 10: McGregor AM et al. Prediction of relapse in hyperthyroid Graves' disease. Lancet 1980; 1:: Sisson JC. Hyaluronic acid in localized myxedema. J Clin Endocrinol Metab 1968;28: From E, Diedrichsen H, Heydenreich G, Nielsen OS. Long acting thyroid stimulator (LATS) and immuno-fluorescent studies in patients with pretibial myxoedema. Dan Med Bull ;20.6: Cheung HS, NicoloffJT, Kamiel MB, Spolter L, Mimni ME. Stimulation of fibroblast biosynthetic activity by serum of patients with pretibial myxoedema. J Invest Dermatol 1978;71: Jollife DS, Gaylarde PM, Brock AP, Sarkany I. Pretibial myxoedema: Stimulation of mucopolysaccharide production of fibroblasts by serum. BrJ Dermatol 1979;100: Konrad K, Brenner W, Pehamberger H. Ultrastructural and immunological findings in Graves' disease with pretibial myxoedema. J Cutan Pathol 1980;7: Selected Writings of Denis Browne by H H Nixon, D Waterston and C A S Wink. 154 pages, illustrated. Trustees of the Sir Denis Browne Memorial Fund. This is a jewel of a book. To have D B's writings gathered together in a volume is an enormous pleasure: at least if you are interested in surgery, paediatrics, paediatric surgery, orthopaedics, urology, plastic surgery, Denis Browne, or a number of other topics, not excluding medical politics. We are given a fascinating collection of tributes from his colleagues which, for me, brought him back to life in an extraordinarily vivid way. I was already installed as his house surgeon in 1950 when Harold Nixon joined the team as registrar, and reading these recollections I just heard his voice again and sensed his presence, with all that it conveyed of commitment, integrity, sharp criticism and sheer fun. I suppose it was a mixture of physique, ability and personality which allowed him to present that extraordinary mixture of Olympian detachment and quite unassuming, even shy, intimacy, which comprised the charm of which Graham Hutton writes in his introductory tribute. It is good to be reminded of such qualities: this book does so. JOHN HOPEWELL
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